Summary: A monitoring programme was established to collect plankton samples and information of environmental variables over the shelf off the island of Gran Canaria during 2005 and 2006. It produced a detailed snapshot of the composition and seasonal assemblages of the decapod larvae community in this locality, in the subtropical waters of the Canary Islands (NE Atlantic), where information about crustacean phenology has been poorly studied. The larval community was mainly composed of benthic taxa, but the contribution of pelagic taxa was also significant. Infraorders Anomura (33.4%) and Caridea (32.8%) accounted for more than half the total collected larvae. High diversity, relatively low larval abundance throughout the year and weak seasonality characterized the annual cycle. However, in relation to the temporal dynamics of temperature, two distinct larval assemblages (cold and warm) were identified that correspond to periods of mixing and stratification of the water column. The results also indicate that larval release times and durations in the subtropical waters are earlier and longer than at other higher latitudes in the NE Atlantic. We detected the presence of larvae of six species that have not yet been reported from the Canary Islands (Pandalina brevirostris, Processa edulis, Necallianasa truncata, Parapenaeus longirostris, Crangon crangon, Nematopagurus longicornis). Finally, this study provides a baseline for future comparisons with respect to fishery pressure and climate variability in this subtropical region.

(where S is the number of species and pi is the proportion of individuals in species i), was used to analyse changes in temporal and spatial diversity in the decapod larvae community. The parametric statistical method (Student t test, p>0.05) was used to evaluate interannual differences in larval abundance and diversity (previously tested for homogeneity of variances using Levene’s test). Multivariate analysis was used to identify larval assemblages with distinct community structure. Only species present in both 2005 and 2006 were used in the analysis in order to eliminate the effect of rare and multispecies groups (e.g. Sergestidae spp., Pagurus spp.). A total of 49 species were left from the initial 105.

After this analysis, using the same Bray-Curtis similarity matrix, a non-metric MDS was performed. The significant results of the SIMPROF test were entered into the MDS plot to assess the level of agreement between the two techniques. Complementarily, the RELATE procedure, employing Spearman rank correlation coefficients (p), was used to determine whether the series of sequential points for mean monthly samples on MDS ordination plots approximated a circle and, if so, the extent to which the distribution of those points was correlated with a true circle (Clarke and Warwick 2001Clarke K., Warwick R. 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd edition: PRIMER-E, Plymouth.). The groups of months detected were used as factors to test significant differences in temporal larval assemblages of decapod species using a one-way similarity analysis (ANOSIM).

Temperature showed a consistent seasonal trend in which the heating due to strong insolation led to maximum values in the mixed layer at 20-30 m (22.9°C in 2005 and 24.1°C in 2006) from August to October. The cooling of the water column started in November and finished around March-April, showing minimum values of 17.7°C in 2015 and 18.3°C in 2016 (Fig. 2). Salinity did not show a seasonal pattern and ranged from 36.54 to 36.97 (Fig. 2). The temporal distribution of chlorophyll a was negatively correlated with temperature (Spearman rank correlation: r=–0.73, p<0.01) and showed the typical seasonality of the Canary Island waters (Table 1, Fig. 2). The quasi-permanent thermocline, which promotes oligotrophic conditions during most of the year and limits phytoplankton production in the Canary Islands (Arístegui et al. 2001Arístegui J., Hernández-León S., Montero M.F., et al. 2001. The seasonal planktonic cycle in coastal waters of the Canary Islands. Sci. Mar. 65: 51-58.), led to standing stocks of chlorophyll a lower than 0.2 mg m–3 during the summer (Fig. 2). This situation changed in winter, when the temperature droped below 19°C and the cooling of the surface eroded the thermocline, promoting the development of a najor phytoplankton bloom in February-March, followed by another smaller peak around April known as the late winter bloom. Interannual differences were observed. The highest chlorophyll a values (0.9 mg m–3) occurred during the bloom of 2005, with a mean standing stock of 0.7±0.16 mg m–3. In 2006 the peak occurred during the same period but was weaker, with a mean standing stock of 0.36±0.05 mg m–3 and maximum values of 0.47 mg m–3. The temporal evolution of temperature suggested different durations of the mixing period. In January 2006 the temperature was still above 19°C, preventing deep convection. In May the heating of the surface waters was already visible, especially in 2006, when the temperature was above 20°C at the beginning of the month. This situation led to a shorter mixing period in 2006 that promoted a lesser phytoplankton bloom.

Fig. 2. – Temporal distribution of temperature (°C), salinity (practical salinity unit, PSU) at 2 m depth, and average chlorophyll a (15-75 m) (mg Chl-a m–3) from January 2005 to December 2006. Vertical profiles of temperature, salinity and chlorophyll a are averaged values for January, May and October.

A total of 6967 larvae belonging to 105 different taxa were identified during the two-year study. Gathered in different suborders, the Pleocyemata and Dendrobranchiata were represented by 85 and 20 taxa, respectively. Within the Pleocyemata, the infraorders with the highest number of taxa were Brachyura (36 taxa) and Caridea (31 taxa). Average species diversity was relatively high (2.40±0.59), with the highest values (>3) in June-August of both years and the lowest (0.60) in January 2005 (Fig. 3). A significant positive correlation with temperature (Spearman rank correlation: r=0.33, p<0.01) was also evidenced this tendency (Table 1). Differences in diversity between years were also significant (Student t test, df=74, t=–2.982,p=0.004), with 2005 showing a lower mean value (2.19±0.86) than 2006 (2.57±0.44).

Fig. 3. – Temporal variation of the abundance (larvae/100 m3) (a) and Shannon–Wiener diversity index (H’) (b) of decapod larvae. Boxplots show yearly comparisons of abundance (c) and diversity (d). In each boxplot, the median (solid line) is indicated in the centre of the box and the edges of the box are the 25th and 75th percentiles; whiskers extend to the most extreme data points that were not considered to be outliers. Results from the Student t test are highlighted as follow: * p<0.05, ** p<0.01.

In terms of relative abundance, the infraorders Anomura and Caridea accounted for 33.4% and 32.8% of the total decapod larvae catches, respectively. Other less abundant taxonomic groups were Brachyura (17.5%), Dendrobranchiata (17.5%), Axiidea and Gebiidea (6%). Achelata and Stenopodidea did not show abundance greater than 5%, while Polychelida, Astacidea, and Glypheidea (this infraorder has not been recorded in the Canary Islands) were not observed in the samples (Table 2). The remaining infraorders are not present in the Canary Islands. The most abundant families within Anomura were Galatheidae (12.2%), Diogenidae (9.2%), and Paguridae (11.8%) due to the main contribution of Galatheaintermedia, Calcinus tubularis and Pagurus spp. (Table 2). In Caridea, the families Apheidae, Hippolytidae and Processidae had abundances of around 7% of the total sample, with Processanouveli and Latreutes fucorum as the most abundant species. The families Brachyura, Majidae, Xanthidae and Grapsidae accounted for around 3% of total abundance. The average abundances of Upogebia spp. (3.8%) and Pandalina brevirostris (3.1%) were also noteworthy. Regarding adult habitat, larvae of benthic species (86.1%) were more abundant than larvae of pelagic species (13.9%) (Table 2). Larvae in the first stage of development, zoea I, accounted for 37.8±13.4% of the total decapod larvae, whereas larvae in the last stage of development always accounted for less than 5% of the total larvae.

Total abundances ranged from a minimum value of 30.2 larvae/100 m3 recorded in February 2005 to the maximum value of 2925 larvae/100 m3 in 12 August 2006. The mean abundance in 2005 (281.02±86.35 larvae/100 m3) was significantly lower (Student t test, df=74, t=–2.07, p=0.021) than in 2006 (478.14±116.13 larvae/100 m3). Decapod larvae were present in the plankton all year round, making it difficult to observe, a priori, any seasonal/interannual patterns (Fig. 3). A two-way ANOSIM test revealed a slight significant difference among months (Global R=0.372, p=0.03) but not among years (Global R=0.133, p=0.4). This result was supported by the MDS plot, which showed a poor spatial ordination of the samples based on their decapod larvae composition (Fig. 4).

Fig. 4. – Non-metric multidimensional scaling ordination based on the Bray-Curtis similarity matrix of decapod larval abundance, using all samples collected in 2005 and 2006.

However, when the factor year was removed and month-averaged larval abundance data were used, the multivariate statistical analysis revealed seasonality in decapod larvae community (Fig. 5). Two significantly different groups of months (p<0.001) were distinguished using SIMPROF at a 58% level of similarity. An MDS plot (2D stress, 0.14) with a superimposed significant cluster shows the separation of the two distinct larval assemblages. A “warm” cluster includes May-September, while the other “cold” cluster includes November-April, and October appears as a transition between the two seasons (Fig. 5). In this ordination, the months tend to undergo a clockwise cyclical spatial distribution (Fig. 5), and RELATE confirmed that the cyclicity was consistent with that of a circle (p=0.001), with a rank correlation coefficient of 0.485. Moreover, the ANOSIM routine revealed that cold and warm larval assemblages were significantly different (Global R=0.489, p=0.002). The average abundance of decapod larvae, temperature, and chlorophyll a are superimposed as proportional bubbles over the MDS plot to visualize the relationship of these variables with the assemblages (Fig. 5), showing that during the warm period the larval abundance is also higher, in agreement with the positive correlation (Spearman rank correlation: r=0.43, p<0.01) between these two variables (Table 1). Conversely, as mention above, chlorophyll a was higher during colder months and therefore negatively correlated (Spearman rank correlation: r=–0.27, p<0.05) with decapod larva abundance.

Fig. 5. – Dendrogram showing the classification of months from the Bray-Curtis similarity matrix of monthly averages of decapod larval abundance (A) Non-metric multidimensional scaling (MDS) ordination based on the same similarity matrix. (B) Average temperature, chlorophyll a, larval abundance and species diversity for each month is superimposed as proportional bubbles over the MDS plot (C-F). Dotted lines separate larval assemblages at the 58% similarity threshold.

This larval assemblage was difficult to visualize in the temporal distribution plot of abundant species, since they were collected in almost every single sampling event, indicating year-round spawning (Figs 6, 7). However, the SIMPER routine revealed that changes in composition and/or abundance were characteristic of the warm and cold assemblages (Table 3). Warm assemblages were found in species that spawn in summer, such as Calcinus tubularis larvaeprimarily collected in summer (54.1±23.8 larvae/100 m3) and Nanocassiope melanodactyla that was abundant during this period (19.4±11.2 larvae/100 m3) (Fig. 6). In the case of the pelagic species Deosergestes henseni, the larvae were collected exclusively in summer and showed a peak around June (19.9±8.8 larvae/100 m3), and Parasergestes vigilax was especially abundant during the summer and autumn of 2006 (Fig. 6). Pachygrapus spp. larvae showed a clear peak (May-October) in 2006 that was not evident in 2005. Other species, such as Alpheus glaber, Clibanarius aequabilis, Percnon gibbesi and Lysmata seticaudata, helped typify the warm assemblage but with lower (<4) similarity percentages (Fig. 6, Table 3). The cold assemblage was characterized by species that exhibited winter-autumn peaks, but their presence in the plankton was not always restricted to cold months. This is the case of Latreutes fucorum (peaks in late summer), and of Eualus occultus, Pandalina brevirostris, and Philocheras bispinosus (peaks in spring-summer) (Fig. 7). Other species that had elevated larval abundance throughout the year (e.g. Processa nouveli, Galathea intermedia, or Lucifer typus) contributed strongly to the cold assemblage but were also important for the warm assemblage (Table 3).

Fig. 6. – Temporal distribution of decapod larval abundance (larvae/100 m3) of typical species of “warm assemblage” during the years 2005 and 2006. Temporal distribution of temperature (°C) at the surface (2 m depth) is also shown. Note that left y-axis scales differ among species.

Fig. 7. – Temporal distribution of decapod larval abundance (larvae/100 m3) of typical species of “cold assemblage” during the years 2005 and 2006. Temporal distribution of temperature (°C) at the surface (2 m depth) is also shown. Note that left y-axis scales differ among species.

Table 3. – Values correspond to the percentage of similarity (SIMPER analysis) of the species that contributed to 80% of average similarity for each assemblage.

Cold
assemblage

Warm
assemblage

Processa nouveli

12.01

8.11

Galathea intermedia

9.52

9.37

Lucifer typus

7.84

4.56

Pandalina brevirostris

6.8

3.02

Latreutes fucorum

6.4

4.03

Pisa tetraodon

5.39

4.48

Alpheus macrocheles

5.26

2.98

Nanocassiope melanodactyla

4.39

8.44

Philocheras sculptus

4.52

Philocheras bispinosus

3.59

Eualus occultus

3.22

Allosergestes pectinatus

3.2

Xantho hydrophilus

3.16

Sergia robusta

3.08

Athanas nitescens

2.07

Calcinus tubularis

11.82

Alpheus glaber

4.63

Ebalia tumefacta

3.36

Deosergestes henseni

3.11

Clibanarius aequabilis

3.05

Percnon gibbesi

2.87

Lysmata seticaudata

2.22

Parasergestes vigilax

2.16

Necallianassa truncata

1.7

New records

We report, for the first time in the Canary Islands waters, the presence of larvae of the species Pandalina brevirostris, Processa edulis, Necallianasa truncata, Parapenaeus longirostris, Crangon crangon and Nematopagurus longicornis. All larval stages of P. brevirostris were found and, as mentioned above, it is an abundant species (mean abundance of 12.21 larvae/100 m3) characterizing the cold assemblage (Fig. 6, Table 3). Processa edulis (zoea I-III stages) was caught in March, May, June-September and November, when it peaked with a mean abundance of 10.18 larvae/100 m3 (Table 2). Larvae of mud shrimp N. truncata (zoea I-III stages) were frequently collected in the plankton, especially in summer, when they achieved significant concentrations in September (mean abundance of 44.46 larvae/100 m3). N. longicornis zoeae III and zoeae IV were observed in March (maximum value of 13.85 larvae/100 m3), July and December 2005 and in January and May 2006. P. longirostris larvae in protozoea III stage of development were observed sporadically in June (3.19 larvae/100 m3) and July (2.61 larvae/100 m3) 2005, and in February and December 2006 (around 7 larvae/100 m3). Only one larva (zoea IV) of C. crangon was caught in January 2006.

This description of the entire larval community of Gran Canaria provides valuable information about the composition and potential spawning season for the most abundant species, which have been largely under-studied. Broadly, the decapod larvae community in Gran Canaria is characterized by contracted larval hatching periods, significant contributions from pelagic species, and weaker seasonality in comparison with higher latitudes, but has two distinct larval assemblages.

This study provides accurate information about the composition and assemblage of decapod larvae in the Canary Islands region. Furthermore, the data collected during this study provide a baseline for future comparisons with respect to fishery pressure and climate variability. Despite the less evident seasonality displayed by most of the species examined, we identify two distinct temporal assemblages of decapod larvae for the subtropical waters of the Canary Islands. Despite significant inter-year differences in diversity and larval abundance, there were no evident changes in the larval assemblages. The detection of such changes in the community requires a multiyear dataset obtained in long-term monitoring programmes (Lindley et al. 2010Lindley J.A., Beaugrand G., Luczak C., et al. 2010. Warm-water decapods and the trophic amplification of climate in the North Sea. Biol. Lett. 6: 773-776.). This may be important, because the temporal distribution of spawning of different species is likely to vary under climate change.

The authors would like to thank all the members of the Biological Oceanography Research Unit of the Universidad de Las Palmas de Gran Canaria who participated in this difficult sampling programme, and S. Hernández-León, principal investigator of the project, for his continuous support. Special thanks are due to J.A. González for providing valuable information about decapod fauna in the Canary Islands and to S. De Grave for his advice during the estimation of the diversity index. The project ConAfrica (CTM2004-02319) of the Spanish Ministry of Science and Innovation funded this study. JML was supported by a postdoctoral fellowship from the Japan Society for Promotion of Science (PE16401).

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